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BACKGROUND: The differentiation of regularly spaced structures within an epithelium is a common feature of developmental pattern formation. The regular spacing of ommatidia in the Drosophila eye imaginal disc provides a good model for this phenomenon. The correct spacing of ommatidia is a central event in establishing the precise hexagonal pattern of ommatidia in the Drosophila compound eye. The R8 photoreceptors are the founder cells of each of the ommatidia that comprise the adult eye and are specified by a bHLH transcription factor, Atonal. RESULTS: We find that the epidermal growth factor receptor (Egfr) has a primary function in regulating R8 spacing. The receptor's activation within nascent ommatidia induces the expression of a secreted inhibitor that blocks atonal expression, and therefore ommatidial initiation, in nearby cells. The identity of the secreted inhibitor remains elusive but, contrary to previous suggestions, we show that it is not Argos. This Egfr-dependent inhibition acts in parallel to the inhibition of atonal by the secreted protein Scabrous. The activation of the Egfr pathway is dependent on Atonal function via the expression of Rhomboid-1. Our results also allow us to conclude that Egfr's role in promoting cell survival is largely independent of its role in photoreceptor recruitment; even when cell death is blocked, most photoreceptors fail to form. CONCLUSIONS: Based on our data and those of others, we propose a model for R8 spacing that comprises a self-organizing network of signaling molecules. This model describes how successive rows of ommatidia form out of phase with each other, leading to the hexagonal array of facets in the compound eye.

Type

Journal article

Journal

Curr Biol

Publication Date

20/03/2001

Volume

11

Pages

396 - 404

Keywords

Animals, Basic Helix-Loop-Helix Transcription Factors, DNA-Binding Proteins, Drosophila Proteins, Drosophila melanogaster, Enzyme Activation, Eye, Eye Proteins, Gene Expression, Glycoproteins, Helix-Loop-Helix Motifs, Insect Proteins, Membrane Proteins, Mitogen-Activated Protein Kinases, Nerve Tissue Proteins, Photoreceptor Cells, Invertebrate, Receptor, Epidermal Growth Factor, Signal Transduction